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Umbilical cord blood acid-base analysis
Dr Fariba Hemmati Neonatologist Associated Professor of Pediatrics SUMS
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Objectives: Become familiar with technique of sampling & normal values for umbilical cord blood gases. Be able to understand the usual relationship between the values in the umbilical vein and the umbilical artery. Be able to recognize when blood samples have been mislabeled. Be able to recognize when asphyxia has been associated with delivery and when it has not. Become reasonably facile with the interpretation of umbilical cord blood gases.
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Background Information:
Blood flows from the placenta to the baby via the umbilical vein, and for the most part enters the ductus venosis, the inferior vena cava, the right atrium, the left artrium (via the foramen ovale), the left ventricle, and the aorta. Blood returns to the placenta via the umbilical arteries. Oxygen is picked up by the fetus from the mother and carbon dioxide is transferred to the mother from the fetus across the intervillous space in the placenta. The blood in the umbilical vein has a predictable relationship with the blood in the umbilical arteries. The blood in the umbilical vein always has the higher pH, the lower PCO2, and the higher PO2.
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Background Information (continued):
Umbilical cord blood gas samples are analyzed for pH, PCO2 and PO2. Bicarbonate, base excess and oxygen saturation are all calculated from the measured parameters. Oxygen saturation is calculated as though the hemoglobin were all hemoglobin A rather than fetal hemoglobin; consequently, the calculated oxygen saturation in umbilical cord blood significantly underestimates the true value. The bicarbonate and the base excess are generally approximately the same in umbilical venous and arterial blood, but if one is worse (a greater metabolic acidosis), it is the arterial blood.
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FETAL ACID-BASE PHYSIOLOGY
Normal fetal metabolism results in the production of acids which are buffered to maintain extracellular pH within a critical range. Very small changes in pH may significantly affect function of various fetal organ systems, such as the central nervous system and the cardiovascular system The fetus produces both volatile (carbonic acid) and nonvolatile acids (organic acids).
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Carbonic acid The fetus produces carbonic acid (H2CO3) during oxidative metabolism (aerobic glycolysis). Carbonic acid dissociates to water and CO2, which readily diffuses across the placenta. Diffusion of CO2 across the placenta is facilitated by a lower PCO2 in the mother during pregnancy, secondary to hyperventilation
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Organic acids organic acids result from fetal anaerobic metabolism
Unlike carbonic acid, the organic acids are cleared very slowly across the placenta and therefore accumulate in the fetus The most important organic acids are lactic acid and ketoacids.
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Buffers The fetus utilizes many different buffers to maintain pH in a very narrow range. The two major buffers are bicarbonate and hemoglobin. The placenta also plays a significant role in helping to maintain a bicarbonate pool and buffering the fetus against changes in maternal pH or blood gas status The level of bicarbonate is important in defining base deficit and base excess.
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Factors affecting fetal acid-base physiology
Maternal perfusion of the placenta and the integrity of the fetal cardiovascular system affect fetal acid-base balance. Rarely, alterations in maternal acid-base balance, such as renal tubular acidosis or diabetic ketoacidosis. fetal pH is normally 0.1 unit lower than that of the mother.
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FETAL VERSUS ADULT ACID-BASE PHYSIOLOGY
Fetal acid-base physiology is similar to that of the adult. There are several notable differences. In the adult, the kidneys and lungs play a significant role in maintaining acid-base balance: respiratory and metabolic acidosis are the result of distinct clinical conditions. By comparison, the fetus depends primarily upon the placenta to act as lungs and, to a lesser degree, kidneys to help compensate for acidemia.
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FETAL VERSUS ADULT ACID-BASE PHYSIOLOGY(continued)
Uteroplacental hypoperfusion is the major cause of both respiratory and metabolic acidemia, with progression from the former to the latter over time If decreased uteroplacental blood flow is not corrected acidosis most likely represents a continuum (mixed acidosis), rather than a distinct clinical entity. Fetal physiology is characterized by inability to compensate for acidemia by compensatory respiratory or renal responses in the same way and to the same degree as in the adult.
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TERMINOLOGY FOR FETAL ACID-BASE DISORDERS
Acidosis — an increase in hydrogen ions in fetal tissue Acidemia — an increase in hydrogen ions in fetal blood. Respiratory acidemia refers to a low pH in the presence of a significantly elevated PCO2 and a normal serum bicarbonate concentration. Metabolic acidemia refers to a low pH with a normal PCO2 and low bicarbonate concentration. A mixed acidemia exists when bicarbonate concentration is low and PCO2 is elevated Hypoxemia — a decrease in oxygen content in fetal blood Hypoxia — a decrease in oxygenation of fetal tissue. Asphyxia — hypoxia with metabolic acidosis. Newborns with hypoxia severe enough to result in hypoxic ischemic encephalopathy (HIE) will usually exhibit an umbilical artery pH of less than 7.00 (often less than 6.90) and a base deficit greater than or equal to 12 mmol/L
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Apgar score and Asphyxia
Historically, asphyxia was defined by a low one-minute and five-minute Apgar score. This was not a reliable criteria because only 30 to 40 percent of newborns who are depressed (ie, have low Apgars) at birth are acidotic at delivery, which suggests that the depression is related to factors other than prolonged hypoxia . Both the American College of Obstetricians and Gynecologists and the American Academy of Pediatrics consider use of the Apgar score in defining asphyxia as a misuse of this scoring system
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Assessment of fetal acid-base balance
in a number of ways: Antepartum umbilical cord blood sampling Fetal scalp blood assessment Umbilical cord blood sampling immediately after delivery
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Antepartum assessment
There is no reliable, noninvasive method prior to delivery. PUBS can be used to determine fetal acid-base during the antepartum period. This technique has been useful in establishing the acid-base profile of fetuses in utero at various gestational ages Its clinical utility is limited because of a high risk of procedure related fetal loss, particularly among fetuses who are compromised, and the need for serial examinations. Therefore, this technique is generally not recommended for antenatal fetal pH assessment.
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Intrapartum assessment
Fetal scalp blood sampling is a direct method of determining pH or lactate concentrations. This technique is rarely performed because it is cumbersome, requires repeated sampling and continuously available laboratory expertise, and is subject to error if there is scalp edema. Furthermore, simple noninvasive procedures, often can provide reassurance of fetal well-being with indirect evidence of the absence of fetal acidosis.
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Assessment at birth Umbilical cord blood sampling at birth provides an objective method of assessing the fetal/newborn acid-base profile and provides useful information about intrapartum fetal status and obstetrical management.
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Umbilical cord blood analysis
Information from umbilical cord blood analysis can also be useful from medical and medicolegal perspectives since it provides insight into intrapartum fetal physiology and, if normal, excludes perinatal asphyxia or hypoxia secondary to the birth process . As an example, only a minority of newborns who have low Apgar scores are acidotic at delivery , which suggests that the depression is related to factors other than prolonged hypoxia
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INDICATIONS There is no consensus regarding indications for umbilical cord blood acid-base analysis postdelivery. It is reasonable to perform this test in the following circumstances: Severe intrauterine growth restriction, multifetal gestations, intrapartum fever, maternal thyroid disease, breech deliveries, and preterm births . Births complicated by meconium staining, an abnormal fetal heart rate pattern, or low five-minute Apgar scores. The RCOG recommend that cord blood acid-base analysis be "considered" for all deliveries.
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TECHNIQUE A 10 to 20 cm segment of umbilical cord is doubly clamped as soon as possible after delivery. Delay in clamping may significantly affect pH and gas values as a result of gaseous diffusion and continuing metabolism. Blood is drawn from the umbilical artery into a 1 to 2 mL syringe, flushed with heparin, and immediately transported on ice to the laboratory. Most studies shown that a cord blood sample in a syringe flushed with heparin and kept on ice is reasonably stable for assessment of both pH and base deficit for 60 minute.
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TECHNIQUE Ideally, the test is performed as soon as possible after delivery. A sample may be obtained immediately and held until a decision is made for or against these tests. Delayed sampling from a clamped umbilical cord at room temperature up to 90 minutes after birth used to estimate the arterial pH and base excess at birth. The estimate is based on studies reporting the rate of fall of pH over time (eg, cord pH falls 0.05 at 30 minutes, at 60 minutes, and 0.11 at 90 minutes after birth).
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TECHNIQUE The pH, PCO2, PO2, CO2, hemoglobin, and oxygen content of the blood can be measured. Bicarbonate concentration, percentage oxygen saturation, and base excess (or deficit) are calculated. The most useful values for interpretation of fetal-newborn condition and prognosis are the pH and base excess (or deficit).
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Normal values The critical pH level that define normal acid-base status is somewhat controversial. The cut-off for significant pathologic acidemia is a pH less than 7.00(may even be less than 6.90). Fetal pH is normally 0.1 unit lower than maternal pH. The mean umbilical blood pH and gas values for premature and term infants are almost identical
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Cesarean delivery & umbilical cord blood gas values
The mean(SD) for umbilical cord blood gas values obtained at cesarean delivery for term pregnancies not in labor were pH 7.27(0.04) pCO2 49(9) mmHg base excess -4(3) mEq/L Slight variations from these values depending on type of anesthesia
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PATHOLOGIC FETAL ACIDEMIA
An exact cutoff to define "significant" acidemia cannot be determined, suggested range of 6.95 to 7.05. A workable threshold for significant or "pathologic fetal acidemia" is 7.00 ,which occurs in 3.7 per 1000 nonanomalous term births ,the overall incidence of neonatal neurologic morbidity or mortality was 23.1 percent in this group. however, that the majority of newborns with pH less than 7.00 will be admitted to the regular newborn nursery and have an uncomplicated neonatal course, and no increased risk for neurologic or behavioral problems when followed to school age.
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PATHOLOGIC FETAL ACIDEMIA
A meta-analysis including a total of 481,753 infants found a relationship between cord pH <7.00 to 7.24 at birth and several adverse neonatal and long-term outcomes: neonatal mortality (OR 16.9, 95% CI ) hypoxic ischemic encephalopathy (OR 13.8, 95% CI ) Intraventricular hemorrhage or periventricular leukomalacia (OR 2.9, 95% CI Cerebral palsy (OR 2.3, 95% CI ) The risk of neonatal morbidity is inversely related to pH with the highest risk at the lowest pHs, especially less than 6.9.
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Umbilical artery PO2 Umbilical artery PO2 is not predictive of any adverse neonatal outcome. Newborns with hypoxia proximate to delivery that might result in subsequent neurologic injury should manifest the following: Umbilical artery blood pH < 7.00 A metabolic component Apgar scores of ≤ 3 for > 5 minutes Seizures, coma, hypotonia Evidence of multisystem organ dysfunction in neonatal period
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Respiratory acidosis Respiratory acidosis alone is not usually associated with complications in the newborn
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Base deficit Metabolic acidosis results in excess production of acid and decreased buffer base, which is referred to as the base deficit. Base deficit does not significantly change during respiratory acidosis. The metabolic component of fetal acidemia (ie, base deficit and bicarbonate) was the most important variable for predicting neonatal morbidity. Base deficit greater than 12 mmol/L is a reasonable threshold for prediction of neonatal complications The risk of moderate or severe newborn complications in newborns with umbilical artery base deficit greater than 16 mmol/L was fourfold higher than in those at 12 to 16 mmol/L (40 and 10 percent, respectively).
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“strong ion difference" (SID)
Base deficit could miss important acid-base abnormalities in complex disturbances encountered during labor and delivery . "strong ion difference" (SID) may permit a more comprehensive approach to acid-base abnormalities in the newborn. SID is defined as (Na+K+Mg+Ca)-(Cl+lactate). No studies have been conducted to relate SID results to neonatal complications.
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Severity and duration of metabolic acidosis
Incidence and severity of newborn complications is related to the severity and duration of metabolic acidosis. A study of term infants who had umbilical cord artery blood pH at birth and within two hours after delivery found the incidence of newborn seizures was highest in the group of infants who had acidemia at birth that persisted through the first two hours of life.
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fetal heart rate patterns
Repetitive moderate or severe variable decelerations may increase the base deficit by 1 mmol/L per 30 minutes Repetitive late or severe atypical variable decelerations (subacute fetal compromise) may increase the base deficit by 1 mmol/L per 6 to 15 minutes; Terminal bradycardia (eg, from ruptured uterus, major abruption, or complete cord occlusion) may increase the base deficit by as much as 1 mmol/L per two to three minutes By comparison, an uncomplicated labor results in a 3 mmol/L change in base deficit over many hours Many factors affect the fetal response to hypoxia; these include an acute versus chronic process, presence of hypotension/hypoperfusion, preterm versus term fetus, presence of anemia or functional cardiovascular anomalies
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Meconium stained amniotic fluid
Meconium stained amniotic fluid (MSAF) complicates approximately 12 percent of pregnancies. In a retrospective review of 766 cases of MSAF from 32 to 42 weeks of gestation, mean umbilical arterial pH did not vary with gestational age, indicating that acidemia is not increased in preterm gestations complicated by meconium passage before birth.
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Lactate levels The umbilical cord blood lactate concentration has also been used as a marker of fetal metabolic acidosis. the mean umbilical artery blood lactate level was / mmol/L (range 0.4 to 5.1 mmol/L) umbilical artery lactate of 5.70 mmol/L had sensitivity and specificity of 69 and 88 percent for moderate or severe HIE.
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LIMITATIONS Fetal blood gas analysis has some limitations that should be considered. Cord blood pH value alone does not distinguish between a primary fetal or placental disorder and the indirect effect of a maternal acid-base disorder. Considering maternal health status and each blood gas value can help define the primary pathologic process. Fetal blood gases also do not necessarily reflect asphyxial processes that occurred remote from delivery or are not global. Lastly, comorbidities (eg, fetal growth restriction, anemia) and duration of insult are important biological modifiers of neurological and other end-organ risk.
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Umbilical Cord Blood Gas Challenge!
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Umbilical Cord Blood Gas Challenge!(Quiz)
In this course's case histories, blood gases are presented using the following shorthand notation: V = 7.35/38/29/-4 A = 7.28/49/18/-4 "A" stands for umbilical artery, "V" stands for umbilical vein. The blood gas values are in the order: pH / PCO2 / PO2 / Base Excess (BE) For example, 7.28/49/18/-4 means pH = 7.28, PCO2 = 49, PO2 = 18, and BE = -4.
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Case #1 Mother - 34 yo G1P0. Uncomplicated IUP at 40.5 weeks. FHR tracing shows mild variables. After 11 hrs of labor taken to DR and delivered a male infant with Apgar scores of 7 at one minute, 9 at 5 minutes. Cord blood gases: V = 7.35/38/29/-4 A = 7.28/49/18/-4 Pick the single best interpretation of the umbilical cord blood gases: Mild respiratory acidosis in the umbilical artery. Mild metabolic acidosis in both umbilical vein and artery. Normal umbilical vein and artery blood gases. Mild respiratory alkalosis in the umbilical vein.
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Normal umbilical vein and artery blood gases.
Venous Arterial PH 7.35 (± 0.05) 7.28 (± 0.05) PCO2 38 (± 5.6) 49 (± 8.4) PO2 29 (± 5.9) 18 (± 6.2) Base Excess -4 (± 2) HCO3 20 (± 2.1) 22 (± 2.5) Accepted norms for umbilical cord blood gase values, as published in American Journal of Obstetrics and Gynecology 151:798, 1985 (N=146)
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Case #2 Mother - 19 yo G2P1Ab1. IUP at 32 wks (poor dates) with preterm labor and diffuse abdominal pain for 4 hours. History of cocaine use, last taken today. FHR monitor reveals repetitive late decelerations, Taken for C/S; thick meconium noted at delivery of 2200 g female infant. Apgar scores were 1 at 1 minute, 2 at 5 minutes, 4 at 10 minutes. Cord blood gases: V 6.85/90/12/15/-23 A 6.80/95/6/14/-25 Pick the single best interpretation of the umbilical cord blood gases: Severe metabolic acidosis, severe respiratory acidosis probably secondary to abruptio placenta. Severe metabolic acidosis, severe respiratory acidosis probably secondary to maternal hypoxemia. Typical blood gas at 32 wks gestation. Probable contamination of sample with meconium.
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Case #3 Mother - 32 yo G4P0Ab3. IUP at 42 wks by fair dates. Presents to triage with breech presentation in active labor with ruptured membranes. Pt taken for C/S. At delivery, some problem delivering the aftercoming head. Apgar scores were 3 at 1 minute, 8 at 5 minutes. Cord blood gases: V 7.19/66/14/-5 A 7.18/68/13/-5 Pick the single best interpretation of the umbilical cord blood gases: Mild respiratory acidosis in both vein and artery. Mild, short duration hypoxemia in both vein and artery. Mild respiratory acidosis and mild, short duration hypoxemia in two samples taken from the same umbilical vessel. Likely A-V anastomosis at level of umbilical cord. None of the above.
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Case #4 Mother - 24 yo G2P0Ab1. IUP at 38 wks. Spontaneous rupture of membranes, in labor. Clear amniotic fluid on admission. FHR shows non-repetitive moderate variable decelerations with an occasional severe variable deceleration. In DR, fetus has deceleration to 60 BPM. Apgar scores are 8 at 1 minute, 9 at 5 minutes. Cord blood gases: V 7.25/52/18/-5 A 7.28/47/29/-5 Pick the single best interpretation of the umbilical cord blood gases: Mislabeling of the umbilical vein and artery samples. Normal vein and artery blood gases. Mild respiratory acidosis in the umbilical vein. None of the above.
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Case #5 Mother - 22 yo G1P0. IUP at 39 wks in active labor. After 6 hours, given fentanyl for pain (refused epidural). Temp 99.8°F, FHR baseline rising. Pushes for 2 hrs without progress and undergoes C/S. Apgar scores are 9 at 1 minute, 9 at 5 minutes. Cord blood gases: V 7.34/38/16/-5 A 7.29/46/14/-15 Pick the single best interpretation of the umbilical cord blood gases: Normal vein and artery blood gases, but with a miscalculation of the base excess in the artery. Metabolic acidosis in the artery probably secondary to lactic acid. Normal vein and artery blood gases. Metabolic acidosis in the artery probably secondary to an acid other than lactic acid. None of the above.
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Case #6 Mother - 38 yo G6P3Ab2. GA=40.5 wks; rule out macrosomia (previous deliveries); morbid obesity. Class A diabetes mellitus, well controlled with diet. Three days PTA had reactive NST. Presents to triage in active labor &SROM with trace meconium. Taken to DR and in 30 min. delivers an infant with Apgar scores of 7 at 1 minute, 9 at 5 minutes. During delivery there was brief difficulty delivering the anterior shoulder. Birth weight was 4675 gm. Cord blood gases: V 7.50/20/92/-4 A 7.26/50/11/-5 Pick the single best interpretation of the umbilical cord blood gases: Moderate respiratory alkalosis in the vein. Short duration hypoxemia in the artery. Maternal hyperventilation while breathing supplemental oxygen resulting in the reported umbilical venous sample. Normal vein and artery blood gases. Contamination of the venous sample with an air bubble.
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Case #7 Mother - 41 yo G4P3. GA=42 wks, with decreased fetal movement since yesterday morning and without any fetal movement today. Presents to hospital .FHR reveals a rate of 140/min, but with a flat baseline (no variability). After 1 hour patient has uncomplicated vaginal delivery of an infant with Apgar scores of 3 at 1 minute, 6 at 5 minutes. Cord blood gases: V 7.35/48/21/-1 A 7.31/52/14/-1 Subsequently in the NICU, the infant had seizure and shows signs of moderate renal failure, which eventually resolves. Pick the single best interpretation of the umbilical cord blood gases: Probable mislabeling of blood gases from the umbilical cord of another infant. Normal vein and artery blood gases. Mild respiratory acidosis in the venous sample with likely resultant decreased perfusion of brain and kidneys. Likely poor resuscitation of an initially borderline infant. None of the above.
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This infant was not suffering from asphyxia at the time of delivery
This infant was not suffering from asphyxia at the time of delivery. Current asphyxia is not the only cause of low Apgar scores. Other causes include severe past asphyxia (which has recovered in utero, but left the baby with current neurologic findings), anesthesia/analgesia, trauma, congenital infection, and congenital neuro/muscular/skeletal diseases, to name a few. The history of decreased fetal movement since yesterday best fits severe past asphyxia or some other disease affecting the CNS that had its onset on the day prior to admission.
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Case #8 Mother - 26 yo G4P4Ab0. IUP at 40 wks. SROM in labor.
Three days PTA, an NST was reactive, but showed several mild variable decelerations. During labor the FHR monitor reveals a spontaneous deceleration to 60 BPM lasting 3 min. Pt taken to the DR, FHR again reveals bradycardia to 60 BPM. Infant delivered by therapeutic outlet forceps. Cord tight around the shoulder and body. Apgar scores are 6 at 1 minute, 9 at 5 minutes. Cord blood gases: V 7.22/52/18/-7 A 7.10/70/10/-11 Pick the single best interpretation of the umbilical cord blood gases: Widened differences (deltas) between venous and arterial samples, likely due to partial occlusion of the umbilical cord. Inadvertent exposure of the arterial sample to exhaled air from a nearby observer. Mild respiratory and mild metabolic acidosis in both venous and arterial samples. Miscalculation of the base excess in the arterial sample. None of these.
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Correct! The umbilical vein is more easily compressed than the artery because it has a thinner muscular wall and the blood pressure in the vein is much lower than that in the artery. When the vein is occluded, blood no longer flows and the baby's blood gas status is no longer reflected in the umbilical venous sample. The cord has little metabolically active tissue, so oxygen is consumed from the occluded venous blood (and CO2 is added to the same blood) only very slowly, and the umbilical venous blood gas values remain relatively unchanged. Meanwhile, the baby continues to pump blood into the placenta through the umbilical artery, gradually becoming hypovolemic, and later, anemic. As long as the artery is not completely occluded, umbilical arterial blood gas values continue to reflect the baby's acid/base status.
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Case #9 Mother - 27 yo G2P1. IUP at 40 wks.
SROM 5 hrs PTA, small amount of clear fluid passed. FHR monitor shows mild variable decelerations. Over the next several hours, the patient progresses & FHR monitor reveals moderate to severe variable decelerations. Vaginal delivery 30 minutes later. Apgar scores are 2 at 1 minute, 2 at 5 minutes, 3 at 10 minutes. Cord blood gases: V 7.31/44/19/-3 A 7.26/53/14/-4 neonate present for resuscitation. Infant intubated and bag ventilated with 100% O2. 30 minutes later, infant's arterial blood gas is: 6.92/87/19/-19. Pick the single best interpretation of the umbilical cord blood gases: Umbilical gases are WNL. Likely presence of hypoplastic lungs with or without unilateral or bilateral pneumothoraces. Umbilical gases are WNL. Likely congenital diaphragmatic hernia. Umbilical artery gas with mild respiratory acidosis and mild hypoxemia of short duration. Likely esophageal intubation. Umbilical gases are WNL. Likely esophageal intubation. Umbilical gases are WNL. Likely cystic adenomatoid malformation.
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Correct The history of only a "small amount" of amniotic fluid when the membranes broke, together with the presence of variable decelerations suggests decreased amniotic fluid volume as is found in Potter's syndrome. Inspection of the placenta may reveal amnion nodosum (bumps on the amnion), which would confirm severe prolonged oligohydramnios. The small colony-like plaques on the amnion are composed of hair, squamous cells, and other debris that is ordinarily suspended in amniotic fluid
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Case #10 Mother - 20 yo G3P1Ab1. IUP at 38 wks. Presents at hospital with UCs, breech presentation with non-pulsatile cord in vagina. Taken for emergent vaginal delivery with low forceps. Delivery of a male infant with Apgar scores of 0 at 1 minute, 0 at 5 minutes, and 0 at 10 minutes. On further questioning, mother states she felt a gush of water while in transit to the hospital. Cord blood gases: V 7.24/55/20/-5 A 7.10/71/8/-10 Attempts to resuscitate the infant are not successful. Umbilical venous blood gas on infant: 6.68/120/6/-30. Pick the single best interpretation of the umbilical cord blood gases: Umbilical gases are obviously not from the patient being discussed. The cord gases do not reflect the severe respiratory and metabolic acidosis of the infant because total cord occlusion from cord prolapse has completely interrupted the flow of blood to and from the placenta. Contamination of the umbilical blood with amniotic fluid. Umbilical venous gas shows a mild respiratory acidosis and the arterial gas a mild metabolic acidosis. Likely undetected esophageal intubation with subsequent poor results.
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Correct! Sudden, complete cord occlusion may result in values that do not reflect the infant's current status, but only the status just before the occlusion. Because there is very little metabolically active tissue in the umbilical cord itself and the cells in the blood specimen do not use much oxygen or produce much carbon dioxide or lactic acid, the values in the sample do not change much over the next half hour or so after the cord is occluded. Note that a sudden complete occlusion without a prior period of partial occlusion is very rare, and in this particular case the widened delta between the arterial and venous samples suggests that there was a brief period of time when the vein was occluded, but the artery was not (i.e. the cord was under some compression, but the pressure was not sufficient to occlude the artery).
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